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Evolution of Carbon Isotope Fractionation in Cyanobacteria

Wang, Renée Z. and Nichols, Robert J. and Liu, Albert K. and Flamholz, Avi I. and Banda, Doug M. and Savage, David F. and Eiler, John M. and Shih, Patrick M. and Fischer, Woodward W. (2022) Evolution of Carbon Isotope Fractionation in Cyanobacteria. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20220706-965519000

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Abstract

The history of Earth’s carbon cycle reflects trends in atmospheric composition convolved with the evolution of photosynthesis. Fortunately, key parts of the carbon cycle have been recorded in the carbon isotope ratios of sedimentary rocks. The dominant model used to interpret this record as a proxy for ancient atmospheric CO₂ is based on carbon isotope fractionations of modern photoautotrophs, and longstanding questions remain about how their evolution might have impacted the record. We interrogated the intersection of environment and evolution by measuring both biomass (εp) and enzymatic (εRubisco) carbon isotope fractionations of a cyanobacterial strain (Synechococcus elongatus PCC 7942) solely expressing a putative ancestral Form 1B rubisco dating to >>1 Ga. This strain, nicknamed ANC, grows in ambient pCO₂ and displays larger εp values than WT, despite having a much smaller ε_(Rubisco) (17.23 ± 0.61‰ vs. 25.18 ± 0.31‰, respectively). Measuring both enzymatic and biomass fractionation revealed a surprising result—ANC εp exceeded ANC εRubisco in all conditions tested, violating prevailing models of cyanobacterial carbon isotope fractionation. However, these models were corrected by accounting for cyanobacterial physiology, notably the CO₂ concentrating mechanism (CCM). Our modified model indicated that powered inorganic carbon uptake systems contribute to ε_p, and this effect is exacerbated in ANC. These data suggested that understanding the evolution of both the CCM and rubisco is critical for interpreting the carbon isotope record, and that large fluctuations in the record may reflect the evolving efficiency of carbon fixing metabolisms as well as changes in atmospheric CO₂.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2022.06.22.497258DOIDiscussion Paper
ORCID:
AuthorORCID
Wang, Renée Z.0000-0003-3994-3244
Nichols, Robert J.0000-0002-8476-0554
Liu, Albert K.0000-0001-9500-0449
Flamholz, Avi I.0000-0002-9278-5479
Banda, Doug M.0000-0001-6198-2923
Savage, David F.0000-0003-0042-2257
Eiler, John M.0000-0001-5768-7593
Shih, Patrick M.0000-0002-2119-3345
Fischer, Woodward W.0000-0002-8836-3054
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. We thank Newton Nguyen for valuable guidance in the MCMC model used to calculate doubling times from growth curve data. We thank Victoria Orphan and Alex Sessions for access to lab space and analytical instruments, as well as lab managers Stephanie A. Connon, Fenfang Wu, and Nami Kitchen for assistance. This research was supported by the David and Lucille Packard Foundation (12540178), Simons Foundation, NASA Exobiology (00010652), and the Schwartz-Reisman Collaborative Science Program (12520057). R.Z.W. was supported by a National Science Foundation Graduate Research Fellowship. Work in the lab of D.F.S. was supported by the US Department of Energy (DE-SC00016240). The authors have declared no competing interest.
Funders:
Funding AgencyGrant Number
David and Lucile Packard Foundation12540178
Simons FoundationUNSPECIFIED
NASA00010652
Schwartz-Reisman Collaborative Science Program12520057
NSF Graduate Research FellowshipUNSPECIFIED
Department of Energy (DOE)DE-SC00016240
Subject Keywords:Evolution, Carbon Isotopes, Rubisco, Cyanobacteria, Precambrian
DOI:10.1101/2022.06.22.497258
Record Number:CaltechAUTHORS:20220706-965519000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220706-965519000
Official Citation:Evolution of Carbon Isotope Fractionation in Cyanobacteria Renée Z. Wang, Robert J. Nichols, Albert K. Liu, Avi I. Flamholz, Doug M. Banda, David F. Savage, John M. Eiler, Patrick M. Shih, Woodward W. Fischer bioRxiv 2022.06.22.497258; doi: https://doi.org/10.1101/2022.06.22.497258
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:115354
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:07 Jul 2022 17:52
Last Modified:07 Jul 2022 17:52

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